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(Received for publication, April 3, 1997, and in revised form, May 1, 1997)
From the Cardiovascular Division, Department of Medicine, Brigham
and Women's Hospital and Harvard Medical School, Boston, Massachusetts
02115
In cardiac myocytes, as well as
specialized conduction and pacemaker cells, agonist binding to
muscarinic acetylcholine receptors (mAchRs) results in the
activation of several signal transduction cascades including the
endothelial isoform of nitric-oxide synthase (eNOS) expressed in these
cells. Recent evidence indicates that, as in endothelial cells, eNOS in
cardiac myocytes is localized to plasmalemma caveolae, specialized
lipid microdomains that contain caveolin-3, a muscle-specific isoform
of the scaffolding protein caveolin. In this report, using a
detergent-free method for isolation of sarcolemmal caveolae from
primary cultures of adult rat ventricular myocytes, we demonstrated
that the muscarinic cholinergic agonist carbachol promotes the
translocation of mAchR into low density gradient fractions containing
most myocyte caveolin-3 and eNOS. Following isopycnic centrifugation,
the different gradient fractions were exposed to the muscarinic
radioligand [3H]quinuclidinyl benzilate (QNB), and
binding was determined after membrane filtration or
immunoprecipitation. In a direct radioligand binding assay, we found
that [3H]QNB binding can be detected in caveolin-enriched
fractions only when cardiac myocytes have been previously exposed to
carbachol. Furthermore, most of this [3H]QNB binding can
be specifically immunoprecipitated by an antibody to the m2 mAchR,
indicating that the translocation of this receptor subtype is
responsible for the [3H]QNB binding detected in the low
density fractions. Moreover, the [3H]QNB binding could be
quantitatively immunoprecipitated from the light membrane fractions
with a caveolin-3 antibody (but not a control IgG1 antibody),
confirming that the m2 mAchR is targeted to caveolae after carbachol
treatment. Importantly, atropine, a muscarinic cholinergic antagonist,
did not induce translocation of m2 mAchR to caveolae and prevented
receptor translocation in response to the agonist carbachol.
Thus, dynamic targeting of sarcolemmal m2 mAchR to caveolae
following agonist binding may be essential to initiate specific
downstream signaling cascades in these cells.
Volume 272, Number 28,
Issue of July 11, 1997
pp. 17744-17748
©1997 by The American Society for Biochemistry and Molecular Biology, Inc.
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Y.-Y. Zhao, O. Feron, C. Dessy, X. Han, M. A. Marchionni, and R. A. Kelly Neuregulin Signaling in the Heart : Dynamic Targeting of erbB4 to Caveolar Microdomains in Cardiac Myocytes Circ. Res., June 25, 1999; 84(12): 1380 - 1387. [Abstract] [Full Text] [PDF]
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R. S. Ostrom and P. A. Insel Caveolar Microdomains of the Sarcolemma : Compartmentation of Signaling Molecules Comes of Age Circ. Res., May 14, 1999; 84(9): 1110 - 1112. [Full Text] [PDF]
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K. E. Loke, P. I. McConnell, J. M. Tuzman, E. G. Shesely, C. J. Smith, C. J. Stackpole, C. I. Thompson, G. Kaley, M. S. Wolin, and T. H. Hintze Endogenous Endothelial Nitric Oxide Synthase–Derived Nitric Oxide Is a Physiological Regulator of Myocardial Oxygen Consumption Circ. Res., April 16, 1999; 84(7): 840 - 845. [Abstract] [Full Text] [PDF]
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C. V. Carman, M. P. Lisanti, and J. L. Benovic Regulation of G Protein-coupled Receptor Kinases by Caveolin J. Biol. Chem., March 26, 1999; 274(13): 8858 - 8864. [Abstract] [Full Text] [PDF]
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R. M. Goetz, H. S. Thatte, P. Prabhakar, M. R. Cho, T. Michel, and D. E. Golan Estradiol induces the calcium-dependent translocation of endothelial nitric oxide synthase PNAS, March 16, 1999; 96(6): 2788 - 2793. [Abstract] [Full Text] [PDF]
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F. Galbiati, D. Volonte, D. Meani, G. Milligan, D. M. Lublin, M. P. Lisanti, and M. Parenti The Dually Acylated NH2-terminal Domain of Gi1alpha Is Sufficient to Target a Green Fluorescent Protein Reporter to Caveolin-enriched Plasma Membrane Domains. PALMITOYLATION OF CAVEOLIN-1 IS REQUIRED FOR THE RECOGNITION OF DUALLY ACYLATED G-PROTEIN alpha SUBUNITS IN VIVO J. Biol. Chem., February 26, 1999; 274(9): 5843 - 5850. [Abstract] [Full Text] [PDF]
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E. A. Ratovitski, M. R. Alam, R. A. Quick, A. McMillan, C. Bao, C. Kozlovsky, T. A. Hand, R. C. Johnson, R. E. Mains, B. A. Eipper, et al. Kalirin Inhibition of Inducible Nitric-oxide Synthase J. Biol. Chem., January 8, 1999; 274(2): 993 - 999. [Abstract] [Full Text] [PDF]
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M. J. Orsini and J. L. Benovic Characterization of Dominant Negative Arrestins That Inhibit beta 2-Adrenergic Receptor Internalization by Distinct Mechanisms J. Biol. Chem., December 18, 1998; 273(51): 34616 - 34622. [Abstract] [Full Text] [PDF]
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O. Feron, C. Dessy, D. J. Opel, M. A. Arstall, R. A. Kelly, and T. Michel Modulation of the Endothelial Nitric-oxide Synthase-Caveolin Interaction in Cardiac Myocytes. IMPLICATIONS FOR THE AUTONOMIC REGULATION OF HEART RATE J. Biol. Chem., November 13, 1998; 273(46): 30249 - 30254. [Abstract] [Full Text] [PDF]
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P. W. Shaul and R. G. W. Anderson Role of plasmalemmal caveolae in signal transduction Am J Physiol Lung Cell Mol Physiol, November 1, 1998; 275(5): L843 - L851. [Abstract] [Full Text] [PDF]
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M. Yamamoto, Y. Toya, C. Schwencke, M. P. Lisanti, M. G. Myers Jr., and Y. Ishikawa Caveolin Is an Activator of Insulin Receptor Signaling J. Biol. Chem., October 9, 1998; 273(41): 26962 - 26968. [Abstract] [Full Text] [PDF]
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 M. J. Polyak, S. H. Tailor, and J. P. Deans Identification of a Cytoplasmic Region of CD20 Required for Its Redistribution to a Detergent-Insoluble Membrane Compartment J. Immunol., October 1, 1998; 161(7): 3242 - 3248. [Abstract] [Full Text] [PDF]
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 N. Ishizaka, K. K. Griendling, B. Lassegue, and R. W. Alexander Angiotensin II Type 1 Receptor : Relationship With Caveolae and Caveolin After Initial Agonist Stimulation Hypertension, September 1, 1998; 32(3): 459 - 466. [Abstract] [Full Text] [PDF]
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T. Drmota, J. Novotny, G.-D. Kim, K. A. Eidne, G. Milligan, and P. Svoboda Agonist-induced Internalization of the G Protein G11alpha and Thyrotropin-releasing Hormone Receptors Proceed on Different Time Scales J. Biol. Chem., August 21, 1998; 273(34): 21699 - 21707. [Abstract] [Full Text] [PDF]
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O. Kifor, R. Diaz, R. Butters, I. Kifor, and E. M. Brown The Calcium-sensing Receptor Is Localized in Caveolin-rich Plasma Membrane Domains of Bovine Parathyroid Cells J. Biol. Chem., August 21, 1998; 273(34): 21708 - 21713. [Abstract] [Full Text] [PDF]
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O. Vogler, G. S. Bogatkewitsch, C. Wriske, P. Krummenerl, K. H. Jakobs, and C. J. van Koppen Receptor Subtype-specific Regulation of Muscarinic Acetylcholine Receptor Sequestration by Dynamin. DISTINCT SEQUESTRATION OF m2 RECEPTORS J. Biol. Chem., May 15, 1998; 273(20): 12155 - 12160. [Abstract] [Full Text] [PDF]
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T. Ikezu, B. D. Trapp, K. S. Song, A. Schlegel, M. P. Lisanti, and T. Okamoto Caveolae, Plasma Membrane Microdomains for alpha -Secretase-mediated Processing of the Amyloid Precursor Protein J. Biol. Chem., April 24, 1998; 273(17): 10485 - 10495. [Abstract] [Full Text] [PDF]
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T. Okamoto, A. Schlegel, P. E. Scherer, and M. P. Lisanti Caveolins, a Family of Scaffolding Proteins for Organizing "Preassembled Signaling Complexes" at the Plasma Membrane J. Biol. Chem., March 6, 1998; 273(10): 5419 - 5422. [Full Text] [PDF]
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H. Tsuga, K. Kameyama, T. Haga, T. Honma, J. Lameh, and W. Sadee Internalization and Down-regulation of Human Muscarinic Acetylcholine Receptor m2 Subtypes. ROLE OF THIRD INTRACELLULAR m2 LOOP AND G PROTEIN-COUPLED RECEPTOR KINASE 2 J. Biol. Chem., February 27, 1998; 273(9): 5323 - 5330. [Abstract] [Full Text] [PDF]
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O. Feron, F. Saldana, J. B. Michel, and T. Michel The Endothelial Nitric-oxide Synthase-Caveolin Regulatory Cycle J. Biol. Chem., February 6, 1998; 273(6): 3125 - 3128. [Abstract] [Full Text] [PDF]
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C. Huang, J. R. Hepler, L. T. Chen, A. G. Gilman, R. G.W. Anderson, and S. M. Mumby Organization of G Proteins and Adenylyl Cyclase at the Plasma Membrane Mol. Biol. Cell, December 1, 1997; 8(12): 2365 - 2378. [Abstract] [Full Text]
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R. Pals-Rylaarsdam, V. V. Gurevich, K. B. Lee, J. A. Ptasienski, J. L. Benovic, and M. M. Hosey Internalization of the m2 Muscarinic Acetylcholine Receptor. ARRESTIN-INDEPENDENT AND -DEPENDENT PATHWAYS J. Biol. Chem., September 19, 1997; 272(38): 23682 - 23689. [Abstract] [Full Text] [PDF]
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K. A. Fagan, K. E. Smith, and D. M. F. Cooper Regulation of the Ca2+-inhibitable Adenylyl Cyclase Type VI by Capacitative Ca2+ Entry Requires Localization in Cholesterol-rich Domains J. Biol. Chem., August 18, 2000; 275(34): 26530 - 26537. [Abstract] [Full Text] [PDF]
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K. S. Murthy and G. M. Makhlouf Heterologous Desensitization Mediated by G Protein-specific Binding to Caveolin J. Biol. Chem., September 22, 2000; 275(39): 30211 - 30219. [Abstract] [Full Text] [PDF]
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M. L. Schlador, R. D. Grubbs, and N. M. Nathanson Multiple Topological Domains Mediate Subtype-specific Internalization of the M2 Muscarinic Acetylcholine Receptor J. Biol. Chem., July 21, 2000; 275(30): 23295 - 23302. [Abstract] [Full Text] [PDF]
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J. Igarashi and T. Michel Agonist-modulated Targeting of the EDG-1 Receptor to Plasmalemmal Caveolae. eNOS ACTIVATION BY SPHINGOSINE 1-PHOSPHATE AND THE ROLE OF CAVEOLIN-1 IN SPHINGOLIPID SIGNAL TRANSDUCTION J. Biol. Chem., October 6, 2000; 275(41): 32363 - 32370. [Abstract] [Full Text] [PDF]
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V. O. Rybin, X. Xu, M. P. Lisanti, and S. F. Steinberg Differential Targeting of beta -Adrenergic Receptor Subtypes and Adenylyl Cyclase to Cardiomyocyte Caveolae. A MECHANISM TO FUNCTIONALLY REGULATE THE cAMP SIGNALING PATHWAY J. Biol. Chem., December 22, 2000; 275(52): 41447 - 41457. [Abstract] [Full Text] [PDF]
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B. Razani, X. L. Zhang, M. Bitzer, G. von Gersdorff, E. P. Bottinger, and M. P. Lisanti Caveolin-1 Regulates Transforming Growth Factor (TGF)-beta /SMAD Signaling through an Interaction with the TGF-beta Type I Receptor J. Biol. Chem., February 23, 2001; 276(9): 6727 - 6738. [Abstract] [Full Text] [PDF]
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Z. Shui, I. A. Khan, T. Haga, J. L. Benovic, and M. R. Boyett Control of the Cardiac Muscarinic K+ Channel by beta -Arrestin 2 J. Biol. Chem., April 6, 2001; 276(15): 11691 - 11697. [Abstract] [Full Text] [PDF]
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J. C. Zwaagstra, M. El-Alfy, and M. D. O'Connor-McCourt Transforming Growth Factor (TGF)-beta 1 Internalization. MODULATION BY LIGAND INTERACTION WITH TGF-beta RECEPTORS TYPES I AND II AND A MECHANISM THAT IS DISTINCT FROM CLATHRIN-MEDIATED ENDOCYTOSIS J. Biol. Chem., July 13, 2001; 276(29): 27237 - 27245. [Abstract] [Full Text] [PDF]
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B. Martinac and O. P. Hamill Gramicidin A channels switch between stretch activation and stretch inactivation depending on bilayer thickness PNAS, April 2, 2002; 99(7): 4308 - 4312. [Abstract] [Full Text] [PDF]
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